Endogenous adaptation to low oxygen modulates T-cell regulatory pathways in EAE

详细信息    查看全文

• 作者：Nilufer Esen ; Vladimir Katyshev ; Zakhar Serkin…
• 关键词：Multiple sclerosis ; EAE ; Hypoxia ; Adaptation ; Angioplasty ; Microvessels ; HIF ; 1α ; IL ; 17 ; T ; regulatory cells
• 刊名：Journal of Neuroinflammation
• 出版年：2016
• 出版时间：December 2016
• 年：2016
• 卷：13
• 期：1
• 全文大小：2,036 KB
• 参考文献：1.Becher B, Segal BM. T(H)17 cytokines in autoimmune neuro-inflammation. Curr Opin Immunol. 2011;23(6):707–12. doi:10.​1016/​j.​coi.​2011.​08.​005 .PubMed PubMedCentral CrossRef
  2.Compston A, Coles A. Multiple sclerosis. Lancet. 2008;372(9648):1502–17. doi:10.​1016/​S0140-6736(08)61620-7 .PubMed CrossRef
  3.Nylander A, Hafler DA. Multiple sclerosis. J Clin Invest. 2012;122(4):1180–8. doi:10.​1172/​JCI58649 .PubMed PubMedCentral CrossRef
  4.Trapp BD, Nave KA. Multiple sclerosis: an immune or neurodegenerative disorder? Annu Rev Neurosci. 2008;31:247–69. doi:10.​1146/​annurev.​neuro.​30.​051606.​094313 .PubMed CrossRef
  5.Balabanov R, Beaumont T, Dore-Duffy P. Role of central nervous system microvascular pericytes in activation of antigen-primed splenic T-lymphocytes. J Neurosci Res. 1999;55(5):578–87.PubMed CrossRef
  6.Dore-Duffy P, Washington R, Dragovic L. Expression of endothelial cell activation antigens in microvessels from patients with multiple sclerosis. Adv Exp Med Biol. 1993;331:243–8.PubMed CrossRef
  7.Fisher M. Injuries to the vascular endothelium: vascular wall and endothelial dysfunction. Rev Neurol Dis. 2008;5 Suppl 1:S4–11.PubMed
  8.Tan KH, Purcell WM, Heales SJ, McLeod JD, Hurst RD. Activated T cells mediate direct blood–brain barrier endothelial cell death and dysfunction. Neuroreport. 2002;13(18):2587–91. doi:10.​1097/​01.​wnr.​0000048544.​12213.​e7 .PubMed CrossRef
  9.Grammas P, Martinez J, Miller B. Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases. Expert Rev Mol Med. 2011;13:e19. doi:10.​1017/​S146239941100191​8 .PubMed CrossRef
  10.Harik N, Harik SI, Kuo NT, Sakai K, Przybylski RJ, LaManna JC. Time-course and reversibility of the hypoxia-induced alterations in cerebral vascularity and cerebral capillary glucose transporter density. Brain Res. 1996;737(1–2):335–8.PubMed CrossRef
  11.Krizanac-Bengez L, Mayberg MR, Janigro D. The cerebral vasculature as a therapeutic target for neurological disorders and the role of shear stress in vascular homeostatis and pathophysiology. Neurol Res. 2004;26(8):846–53.PubMed CrossRef
  12.Lassmann H. Hypoxia-like tissue injury as a component of multiple sclerosis lesions. J Neurol Sci. 2003;206(2):187–91.PubMed CrossRef
  13.Trapp BD, Stys PK. Virtual hypoxia and chronic necrosis of demyelinated axons in multiple sclerosis. Lancet Neurol. 2009;8(3):280–91. doi:10.​1016/​S1474-4422(09)70043-2 .PubMed CrossRef
  14.Dore-Duffy P, LaManna JC. Physiologic angiodynamics in the brain. Antioxid Redox Signal. 2007;9(9):1363–71. doi:10.​1089/​ars.​2007.​1713 .PubMed CrossRef
  15.Hawkins BT, Davis TP. The blood–brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57(2):173–85. doi:10.​1124/​pr.​57.​2.​4 .PubMed CrossRef
  16.Ward NL, LaManna JC. The neurovascular unit and its growth factors: coordinated response in the vascular and nervous systems. Neurol Res. 2004;26(8):870–83.PubMed CrossRef
  17.Ding YH, Ding Y, Li J, Bessert DA, Rafols JA. Exercise pre-conditioning strengthens brain microvascular integrity in a rat stroke model. Neurol Res. 2006;28(2):184–9. doi:10.​1179/​016164106X98053 .PubMed CrossRef
  18.Padilla J, Simmons GH, Bender SB, Arce-Esquivel AA, Whyte JJ, Laughlin MH. Vascular effects of exercise: endothelial adaptations beyond active muscle beds. Physiology (Bethesda). 2011;26(3):132–45. doi:10.​1152/​physiol.​00052.​2010 .CrossRef
  19.Zheng Q, Zhu D, Bai Y, Wu Y, Jia J, Hu Y. Exercise improves recovery after ischemic brain injury by inducing the expression of angiopoietin-1 and Tie-2 in rats. Tohoku J Exp Med. 2011;224(3):221–8. doi:10.​1620/​tjem.​224.​221 .PubMed CrossRef
  20.Berchtold NC, Castello N, Cotman CW. Exercise and time-dependent benefits to learning and memory. Neuroscience. 2010;167(3):588–97. doi:10.​1016/​j.​neuroscience.​2010.​02.​050 .PubMed PubMedCentral CrossRef
  21.Koutsioumpa M, Drosou G, Mikelis C, Theochari K, Vourtsis D, Katsoris P, et al. Pleiotrophin expression and role in physiological angiogenesis in vivo: potential involvement of nucleolin. Vasc Cell. 2012;4:4. doi:10.​1186/​2045-824X-4-4 .PubMed PubMedCentral CrossRef
  22.Xu K, LaManna JC. Chronic hypoxia and the cerebral circulation. J Appl Physiol. 2006;100(2):725–30. doi:10.​1152/​japplphysiol.​00940.​2005 .PubMed CrossRef
  23.Dore-Duffy P, Balabanov R, Beaumont T, Hritz MA, Harik SI, LaManna JC. Endothelial activation following prolonged hypobaric hypoxia. Microvasc Res. 1999;57(2):75–85. doi:10.​1006/​mvre.​1998.​2112 .PubMed CrossRef
  24.Dore-Duffy P, Balabanov R, Beaumont T, Katar M. The CNS pericyte response to low oxygen: early synthesis of cyclopentenone prostaglandins of the J-series. Microvasc Res. 2005;69(1–2):79–88. doi:10.​1016/​j.​mvr.​2004.​11.​004 .PubMed CrossRef
  25.Dore-Duffy P, Wencel M, Katyshev V, Cleary K. Chronic mild hypoxia ameliorates chronic inflammatory activity in myelin oligodendrocyte glycoprotein (MOG) peptide induced experimental autoimmune encephalomyelitis (EAE). Adv Exp Med Biol. 2011;701:165–73. doi:10.​1007/​978-1-4419-7756-4_​23 .PubMed CrossRef
  26.Esen N, Blakely PK, Rainey-Barger EK, Irani DN. Complexity of the microglial activation pathways that drive innate host responses during lethal alphavirus encephalitis in mice. ASN Neuro. 2012;4(4):207–21. doi:10.​1042/​AN20120016 .PubMed CrossRef
  27.Varia MA, Calkins-Adams DP, Rinker LH, Kennedy AS, Novotny DB, Fowler Jr WC, et al. Pimonidazole: a novel hypoxia marker for complementary study of tumor hypoxia and cell proliferation in cervical carcinoma. Gynecol Oncol. 1998;71(2):270–7. doi:10.​1006/​gyno.​1998.​5163 .PubMed CrossRef
  28.Selvaraj RK, Geiger TL. Mitigation of experimental allergic encephalomyelitis by TGF-beta induced Foxp3+ regulatory T lymphocytes through the induction of anergy and infectious tolerance. J Immunol. 2008;180(5):2830–8.PubMed CrossRef
  29.Trandem K, Anghelina D, Zhao J, Perlman S. Regulatory T cells inhibit T cell proliferation and decrease demyelination in mice chronically infected with a coronavirus. J Immunol. 2010;184(8):4391–400. doi:10.​4049/​jimmunol.​0903918 .PubMed PubMedCentral CrossRef
  30.Dziurla R, Gaber T, Fangradt M, Hahne M, Tripmacher R, Kolar P, et al. Effects of hypoxia and/or lack of glucose on cellular energy metabolism and cytokine production in stimulated human CD4+ T lymphocytes. Immunol Lett. 2010;131(1):97–105. doi:10.​1016/​j.​imlet.​2010.​02.​008 .PubMed CrossRef
  31.Dace DS, Khan AA, Kelly J, Apte RS. Interleukin-10 promotes pathological angiogenesis by regulating macrophage response to hypoxia during development. PLoS One. 2008;3(10):e3381. doi:10.​1371/​journal.​pone.​0003381 .PubMed PubMedCentral CrossRef
  32.Apte RS, Richter J, Herndon J, Ferguson TA. Macrophages inhibit neovascularization in a murine model of age-related macular degeneration. PLoS Med. 2006;3(8):e310. doi:10.​1371/​journal.​pmed.​0030310 .PubMed PubMedCentral CrossRef
  33.Huang WX, Huang P, Link H, Hillert J. Cytokine analysis in multiple sclerosis by competitive RT - PCR: a decreased expression of IL-10 and an increased expression of TNF-alpha in chronic progression. Mult Scler. 1999;5(5):342–8.PubMed
  34.Rubenstein JL, Wong VS, Kadoch C, Gao HX, Barajas R, Chen L, et al. CXCL13 plus interleukin 10 is highly specific for the diagnosis of CNS lymphoma. Blood. 2013;121(23):4740–8. doi:10.​1182/​blood-2013-01-476333 .PubMed PubMedCentral CrossRef
  35.Cannella B, Gao YL, Brosnan C, Raine CS. IL-10 fails to abrogate experimental autoimmune encephalomyelitis. J Neurosci Res. 1996;45(6):735–46. doi:10.​1002/​(SICI)1097-4547(19960915)45:​6<735:​:​AID-JNR10>3.​0.​CO;2-V .PubMed CrossRef
  36.Festa ED, Hankiewicz K, Kim S, Skurnick J, Wolansky LJ, Cook SD, et al. Serum levels of CXCL13 are elevated in active multiple sclerosis. Mult Scler. 2009;15(11):1271–9. doi:10.​1177/​1352458509107017​ .PubMed CrossRef
  37.Kowarik MC, Cepok S, Sellner J, Grummel V, Weber MS, Korn T, et al. CXCL13 is the major determinant for B cell recruitment to the CSF during neuroinflammation. J Neuroinflammation. 2012;9:93. doi:10.​1186/​1742-2094-9-93 .PubMed PubMedCentral CrossRef
  38.Bagaeva LV, Rao P, Powers JM, Segal BM. CXC chemokine ligand 13 plays a role in experimental autoimmune encephalomyelitis. J Immunol. 2006;176(12):7676–85.PubMed CrossRef
  39.Rainey-Barger EK, Rumble JM, Lalor SJ, Esen N, Segal BM, Irani DN. The lymphoid chemokine, CXCL13, is dispensable for the initial recruitment of B cells to the acutely inflamed central nervous system. Brain Behav Immun. 2011;25(5):922–31. doi:10.​1016/​j.​bbi.​2010.​10.​002 .PubMed PubMedCentral CrossRef
  40.Gaupp S, Pitt D, Kuziel WA, Cannella B, Raine CS. Experimental autoimmune encephalomyelitis (EAE) in CCR2(−/−) mice: susceptibility in multiple strains. Am J Pathol. 2003;162(1):139–50. doi:10.​1016/​S0002-9440(10)63805-9 .PubMed PubMedCentral CrossRef
  41.Schmitt C, Strazielle N, Ghersi-Egea JF. Brain leukocyte infiltration initiated by peripheral inflammation or experimental autoimmune encephalomyelitis occurs through pathways connected to the CSF-filled compartments of the forebrain and midbrain. J Neuroinflammation. 2012;9:187. doi:10.​1186/​1742-2094-9-187 .PubMed PubMedCentral CrossRef
  42.Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, et al. Differential roles of microglia and monocytes in the inflamed central nervous system. J Exp Med. 2014;211(8):1533–49. doi:10.​1084/​jem.​20132477 .PubMed PubMedCentral CrossRef
  43.LaManna JC, Chavez JC, Pichiule P. Structural and functional adaptation to hypoxia in the rat brain. J Exp Biol. 2004;207(Pt 18):3163–9. doi:10.​1242/​jeb.​00976 .PubMed CrossRef
  44.Nilsson M, Heymach JV. Vascular endothelial growth factor (VEGF) pathway. J Thorac Oncol. 2006;1(8):768–70.PubMed CrossRef
  45.Mengozzi M, Cervellini I, Bigini P, Martone S, Biondi A, Pedotti R, et al. Endogenous erythropoietin as part of the cytokine network in the pathogenesis of experimental autoimmune encephalomyelitis. Mol Med. 2008;14(11–12):682–8. doi:10.​2119/​2008-00086.​Mengozzi .PubMed PubMedCentral
  46.Pan F, Barbi J, Pardoll DM. Hypoxia-inducible factor 1: a link between metabolism and T cell differentiation and a potential therapeutic target. Oncoimmunology. 2012;1(4):510–5.PubMed PubMedCentral CrossRef
  47.Colgan SP, Taylor CT. Hypoxia: an alarm signal during intestinal inflammation. Nat Rev Gastroenterol Hepatol. 2010;7(5):281–7. doi:10.​1038/​nrgastro.​2010.​39 .PubMed PubMedCentral CrossRef
  48.McNamee EN, Korns Johnson D, Homann D, Clambey ET. Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol Res. 2012. doi:10.​1007/​s12026-012-8349-8 .
  49.Davies AL, Desai RA, Bloomfield PS, McIntosh PR, Chapple KJ, Linington C, et al. Neurological deficits caused by tissue hypoxia in neuroinflammatory disease. Ann Neurol. 2013;74(6):815–25. doi:10.​1002/​ana.​24006 .PubMed CrossRef
  50.Austin MA, Wills KE, Blizzard L, Walters EH, Wood-Baker R. Effect of high flow oxygen on mortality in chronic obstructive pulmonary disease patients in prehospital setting: randomised controlled trial. BMJ. 2010;341:c5462. doi:10.​1136/​bmj.​c5462 .PubMed PubMedCentral CrossRef
  51.Barbi J, Pardoll D, Pan F. Metabolic control of the Treg/Th17 axis. Immunol Rev. 2013;252(1):52–77. doi:10.​1111/​imr.​12029 .PubMed PubMedCentral CrossRef
  52.Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR, et al. HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med. 2011;208(7):1367–76. doi:10.​1084/​jem.​20110278 .PubMed PubMedCentral CrossRef
  53.Clambey ET, McNamee EN, Westrich JA, Glover LE, Campbell EL, Jedlicka P, et al. Hypoxia-inducible factor-1 alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci U S A. 2012;109(41):E2784–93. doi:10.​1073/​pnas.​1202366109 .PubMed PubMedCentral CrossRef
  54.Nakamura H, Makino Y, Okamoto K, Poellinger L, Ohnuma K, Morimoto C, et al. TCR engagement increases hypoxia-inducible factor-1 alpha protein synthesis via rapamycin-sensitive pathway under hypoxic conditions in human peripheral T cells. J Immunol. 2005;174(12):7592–9.PubMed CrossRef
  55.Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. 2009;9(9):609–17. doi:10.​1038/​nri2607 .PubMed PubMedCentral CrossRef
  56.Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, Kakuta S, et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol. 2006;177(1):566–73.PubMed CrossRef
  57.Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med. 2005;201(2):233–40. doi:10.​1084/​jem.​20041257 .PubMed PubMedCentral CrossRef
  58.McGeachy MJ, Stephens LA, Anderton SM. Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. J Immunol. 2005;175(5):3025–32.PubMed CrossRef
  59.Segal BM. The unwavering commitment of regulatory T cells in the suppression of autoimmune encephalomyelitis: another aspect of immune privilege in the CNS. Eur J Immunol. 2012;42(5):1102–5. doi:10.​1002/​eji.​201242567 .PubMed CrossRef
  60.Chen L, Coleman R, Leang R, Tran H, Kopf A, Walsh Craig M et al. Human neural precursor cells promote neurologic recovery in a viral model of multiple sclerosis. Stem Cell Reports. 2014;2(6):825–37. doi:http://​dx.​doi.​org/​10.​1016/​j.​stemcr.​2014.​04.​005 .
  61.Ragheb S, Li Y, Simon K, VanHaerents S, Galimberti D, De Riz M, et al. Multiple sclerosis: BAFF and CXCL13 in cerebrospinal fluid. Mult Scler. 2011;17(7):819–29. doi:10.​1177/​1352458511398887​ .PubMed CrossRef
  62.Brettschneider J, Czerwoniak A, Senel M, Fang L, Kassubek J, Pinkhardt E, et al. The chemokine CXCL13 is a prognostic marker in clinically isolated syndrome (CIS). PLoS One. 2010;5(8):e11986. doi:10.​1371/​journal.​pone.​0011986 .PubMed PubMedCentral CrossRef
  63.Alvarez E, Piccio L, Mikesell RJ, Klawiter EC, Parks BJ, Naismith RT, et al. CXCL13 is a biomarker of inflammation in multiple sclerosis, neuromyelitis optica, and other neurological conditions. Mult Scler. 2013;19(9):1204–8. doi:10.​1177/​1352458512473362​ .PubMed PubMedCentral CrossRef
  64.Schreml S, Szeimies RM, Prantl L, Karrer S, Landthaler M, Babilas P. Oxygen in acute and chronic wound healing. Br J Dermatol. 2010;163(2):257–68. doi:10.​1111/​j.​1365-2133.​2010.​09804.​x .PubMed CrossRef
  65.Xing D, Liu L, Marti GP, Zhang X, Reinblatt M, Milner SM, et al. Hypoxia and hypoxia-inducible factor in the burn wound. Wound repair and regeneration: official publication of the Wound Healing Society [and] the European Tissue Repair. Society. 2011;19(2):205–13. doi:10.​1111/​j.​1524-475X.​2010.​00656.​x .
  66.Zampell JC, Yan A, Avraham T, Daluvoy S, Weitman ES, Mehrara BJ. HIF-1alpha coordinates lymphangiogenesis during wound healing and in response to inflammation. FASEB J. 2012;26(3):1027–39. doi:10.​1096/​fj.​11-195321 .PubMed PubMedCentral CrossRef
  67.Hayes HB, Jayaraman A, Herrmann M, Mitchell GS, Rymer WZ, Trumbower RD. Daily intermittent hypoxia enhances walking after chronic spinal cord injury: a randomized trial. Neurology. 2014;82(2):104–13. doi:10.​1212/​01.​WNL.​0000437416.​34298.​43 .PubMed PubMedCentral CrossRef
  
• 作者单位：Nilufer Esen (1)
  Vladimir Katyshev (1)
  Zakhar Serkin (1)
  Svetlana Katysheva (1)
  Paula Dore-Duffy (1)
  
  1. Department of Neurology, School of Medicine, Wayne State University, Detroit, MI, 48201, USA
  
• 刊物主题：Neurosciences; Neurology; Neurobiology; Immunology;
• 出版者：BioMed Central
• ISSN：1742-2094

文摘

Background In the brain, chronic inflammatory activity may lead to compromised delivery of oxygen and glucose suggesting that therapeutic approaches aimed at restoring metabolic balance may be useful. In vivo exposure to chronic mild normobaric hypoxia (10 % oxygen) leads to a number of endogenous adaptations that includes vascular remodeling (angioplasticity). Angioplasticity promotes tissue survival. We have previously shown that induction of adaptive angioplasticity modulates the disease pattern in myelin oligodendrocyte glycoprotein (MOG)-induced experimental autoimmune encephalomyelitis (EAE). In the present study, we define mechanisms by which adaptation to low oxygen functionally ameliorates the signs and symptoms of EAE and for the first time show that tissue hypoxia may fundamentally alter neurodegenerative disease.